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OBJECTIVES: To determine whether lower lean mass CONCLUSION: In this older cohort, lower strength
and higher fat mass have independent effects on the loss of with older age was predominantly due to a lower muscle
strength and muscle quality in older adults and might ex- mass. Age and body fat also had significant inverse associ-
plain part of the effect of age. ations with strength and muscle quality. Both preservation
DESIGN: Single-episode, cross-sectional analyses of a co- of lean mass and prevention of gain in fat may be impor-
hort of subjects in the Health, Aging and Body Composi- tant in maintaining strength and muscle quality in old age.
tion (Health ABC) Study. J Am Geriatr Soc 51:323330, 2003.
SETTING: Ambulatory clinic and research laboratory. Key words: strength; muscle quality; sarcopenia; aging
PARTICIPANTS: Two thousand six hundred twenty-
three men and women aged 70 to 79 from the Health ABC
Study.
MEASUREMENTS: Upper and lower extremity strength
was measured using isokinetic (knee extension) and iso-
metric (grip strength) dynamometers. Body composition
(lean mass and fat mass) was determined by measuring
T he loss in muscle mass with age, referred to as sar-
copenia, is a major contributor to decreased strength
in older adults. Strength is closely related to muscle size, so
lean mass of upper and lower extremities and the total loss of muscle mass will result in loss of strength. Muscle
body by dual-energy x-ray absorptiometry. Muscle quality size in turn is related to overall body size, so taller or more
was ascertained by taking the ratio of strength to muscle obese individuals tend to be stronger than shorter or thin-
mass for both upper and lower extremities. ner individuals on the basis of size alone. Before the ad-
RESULTS: Upper and lower extremity strength and mus- vent of newer methods of body composition assessment,
cle quality decreased as age increased. Most of the ex- muscle size was difficult to determine precisely in popula-
plained variance in strength was due to differences in mus- tion studies. With the use of computed tomography (CT)
cle mass, but, in those at the extremes of body fat and scanning and dual-energy x-ray absorptiometry (DEXA)
lower leg muscle quality, the association with body fat muscle area, mass, and other aspects of body composition
was independent of the effect of age. Although blacks had can now be measured directly in large cohort studies.
greater muscle strength and mass than whites, leg muscle Some studies show that the loss of strength is some-
quality tended to be lower in blacks than in whites. Upper what greater than loss of muscle mass with aging,18 im-
extremity strength adjusted for lean mass and muscle qual- plying that the quality of the muscle remaining may be re-
ity were also associated inversely and independently with duced. Accompanying the loss of lean mass with age is an
age, body fat, and black race. increase in fat mass, so the percentage of body fat is higher
in older adults, even if weight is not.9 With increasing obe-
From the *Department of Medicine, University of Pittsburgh, Pittsburgh, sity, the proportion of body composition that is fat increases
Pennsylvania; Epidemiology, Demography and Biometry Program, Na- more than the proportion that is lean. As with older indi-
tional Institute on Aging, Bethesda, Maryland; Department of Preventive viduals, obese individuals have also been shown to be
Medicine, University of Tennessee, Memphis, Tennessee; Preventive Sciences
Group, University of California at San Francisco, San Francisco, California; weaker than would be expected for their size.10 Although
Department of Family Practice, University of Texas, San Antonio, Texas; and there are few physiological data available to support a spe-
Institute for Research in Extramural Medicine, Vrije Universiteit, Amsterdam,
cific mechanism for these observations, it seems plausible
the Netherlands. that higher body fat in older adults might account for part
Supported by National Institute on Aging Contracts N01-AG-62101,
of the effect of age on muscle quality.11
N01-AG-62103, and N01-AG-62106.
The Health, Aging and Body Composition (Health
Address correspondence to Anne B. Newman, MD, MPH, 3520 5th
Avenue, Suite 300, University of Pittsburgh School of Medicine, Division of ABC) Study was designed to characterize body composition
Geriatric Medicine, Pittsburgh, PA 15213. E-mail: anewman@pitt.edu and strength in a large population of well-functioning men
and women to evaluate factors that might be associated testing also had grip strength testing. For these analyses,
with loss of strength and muscle mass and incident func- the maximum of the force from two trials was used for the
tional limitation. This cross-sectional analysis describes right upper extremity.
strength, muscle mass, and muscle quality in relationship
to age, race, and body composition. The authors hypothe- Body Composition
sized that strength and muscle quality would be reduced
Lean mass of the upper and lower extremities and the total
with age and that lower muscle mass and higher body fat
body was assessed using DEXA (Hologic QDR 4500, soft-
might independently influence this relationship.
ware version 8.21, Bedford, MA). The legs were defined
using a line bisecting the femoral neck and the arms by a
METHODS line through the head of the humerus and the scapula.
Population Bone mineral content was subtracted from the total and
regional lean mass to define total nonbone lean mass,
The Health ABC Study cohort includes 3,075 men (48.4%) which represents primarily skeletal muscle in the extremi-
and women (51.6%) aged 70 to 79, of whom 41.6% are ties.12 Fat mass was estimated for the whole body as well.
African American. Whites were recruited from a random Both the percentage of fat and total fat were examined in
sample of Medicare beneficiaries in ZIP codes in Pitts- these analyses. Body weight and height were measured in a
burgh, Pennsylvania, and Memphis, Tennessee, and blacks hospital gown with no shoes using a calibrated balance
were recruited from all age-eligible people in these areas. beam scale and stadiometer, respectively. Body mass index
Sampled participants received a mailing followed by a tele- (BMI) in kg/m2 was also examined as a measure of body
phone eligibility screen. Eligibility criteria included age 70 composition. Finally, analyses for the lower extremity
to 79 during the recruitment period (March 1997 to July were repeated using CT scan cross-sectional muscle area. 13
1998), self-report of no difficulty walking one-quarter of a
mile or climbing 10 steps, no difficulty with basic activities
Muscle Quality
of daily living, no history of active treatment for cancer in
the prior 3 years, and no plan to move out of the area in Similar to other reports in the literature, a measure of mus-
the next 3 years. Those eligible were recruited for a 4- to cle quality was created by taking the ratio of strength to
5-hour comprehensive examination. All participants gave muscle mass for the upper and lower extremities. For the
informed consent, and the institutional review boards at lower extremity, the term specific torque is used for the
each field center approved the consent forms and protocol. ratio of isokinetic torque in N-m at the knee to leg lean
For the present analysis, only those with complete data for mass in kg by DEXA. For the upper extremity, strength
isokinetic torque and body composition were included (n was measured in kg of force, thus the term specific force is
2,623); exclusions are discussed below. used to describe the ratio of grip strength to arm lean mass.
Other Covariates
Strength Assessments
Physical activity, the total number of chronic conditions,
Strength was measured in the lower and upper extremities, smoking, and site were all included in the final models as
using an isokinetic dynamometer (Kin-Com dynamometer, possible confounders of the effects of age or race on strength
125 AP, Chattanooga, TN) for knee extension and an iso- and muscle quality. Physical activity was assessed by self-
metric dynamometer (Jaymar, JLW Instruments, Chicago, report as total kcal/wk expended on walking and exercise.14
IL) for grip strength. For knee extension, the right leg was Smoking history was assessed by questionnaire and classi-
used unless contraindicated by pain or history of joint re- fied as current, past, or never smokers. Comorbidity was as-
placement. Participants with uncontrolled hypertension, sessed as the total number of 11 chronic health conditions,
stroke, bilateral knee replacement, or severe bilateral knee using self-report with confirmation by treatment and medi-
pain were excluded from the test, resulting in exclusion of cations. These included cancer, myocardial infarction, con-
401 (13%) of the cohort. Those who were excluded were gestive heart failure, depression, diabetes mellitus, hyperten-
of similar sex (48.9% men vs 51.1% women, P .22) and sion, knee osteoarthritis, osteoporosis, peripheral arterial
race (50% blacks vs 50% whites, P .45), and were disease, pulmonary disease, and stomach/duodenal ulcer.
slightly older (mean age 74.0 vs 73.6 years, P .003) but
of similar body composition to those who were tested.
Statistical Analysis
Maximal voluntary concentric isokinetic torque was
assessed in Newton-meters (N-m) at 60/s angular veloc- Distributions were examined separately in men and women
ity. Start and stop angles were set at 90 and 30. At least and by race. The specific torque and force ratios were nor-
three, but no more than six, maximal efforts were allowed mally distributed. The relationships between (1) muscle
to produce three overlying curves, and the mean maximal strength, lean mass, and specific torque and (2) age and fat
torque production was recorded. An interexaminer reliabil- mass were examined separately in men and women by
ity study in 60 participants showed no significant differences race, using analysis of variance, and by inspection of scat-
between examiners and a within-participant coefficient of terplots and moving average plots. Analyses are presented
variation of about 11%. There was also a significant site by sex, because there was little overlap in body composi-
difference, so models were adjusted for study site. tion between men and women. Interactions with race
Isometric grip strength was assessed for each hand. within sex were examined; none were found. Multiple lin-
Participants with severe hand pain or recent surgery were ear regression was used to examine the relationship be-
excluded. The vast majority (96%) who had leg strength tween strength and lean mass, adjusting for age, race, and
JAGS MARCH 2003VOL. 51, NO. 3 STRENGTH AND MUSCLE QUALITY 325
Table 1. Characteristics of Participants: The Health, Aging and Body Composition Study
White Men Black Men All Men White Women Black Women All Women Total
n 827 n 459 n 1,286 n 743 n 594 n 1,337 N 2,623
Age 73.9 2.9 73.4 2.8 73.7 2.9* 73.5 2.8 73.3 2.9 73.4 2.8* 73.6 2.9
Height, m 1.7 0.06 1.7 0.07 1.7 0.07* 1.6 0.06 1.6 0.06 1.6 0.06* 1.7 0.09
Weight, kg 81.2 12.3 81.6 14.4 81.4 13.1* 66.3 12.3 75.5 15.4 70.4 14.5* 75.8 14.9
Body mass 27.0 3.7 27.2 4.3 27.0 3.9* 26.0 4.6 29.6 5.7 27.6 5.4* 27.3 4.7
index, kg/m2
Total % fat 26.1 4.9 24.0 5.6 25.3 5.2* 36.8 5.8 37.9 6.2 37.3 6.0* 31.4 8.2
Total fat, kg 21.7 6.7 20.3 7.3 21.2 7.0* 25.1 7.8 29.5 9.8 27.1 9.0* 24.2 8.6
Leg torque, Nm 130.55 30.67 135.04 36.99 132.15 33.12* 78.60 19.57 85.91 23.23 81.85 21.57* 106.51 37.52
Leg lean 9.01 1.24 9.67 1.55 9.24 1.40* 6.21 1.01 7.34 1.30 6.72 1.28* 7.95 1.84
mass, kg
Specific torque, 14.51 2.88 14.04 3.41 14.35 3.09* 12.73 2.74 11.90 3.14 12.36 2.95* 13.33 3.18
Nm/kg
*Gender difference at P .01.
Racial difference at P .05.
Table 2. Leg Strength, Leg Lean Mass, and Muscle Quality by Age
Age
0.03 0.004*
1.31 0.19*
1.04 0.50*
9.23 0.64*
1.22 0.27*
0.30 1.19
greater strength and lean mass in black men and women,
Model 4
0.2840
unadjusted leg muscle quality (specific torque) was lower
than in their white counterparts.
Even in this rather narrow age range, those who were
older had significantly lower strength and lean mass (Ta-
ble 2). The associations with age were somewhat stronger
for leg strength than for leg lean mass, resulting in a signif-
0.03 0.004*
1.33 0.19*
9.20 0.64*
1.25 0.26*
icant inverse relationship between lower extremity specific
0.80 1.17
Model 3
0.2403
torque and age. Leg lean mass was lower by about 0.1 kg
per year of age, or about 9% to 10% lower across the de-
cade of age in both men and women. Leg strength was
Women
lower by 2.5 N-m per year of age in men and 1.8 N-m per
year in women, across the decade of age.
The coefficient (standard error) for age in relation-
1.29 0.19*
6.58 0.47*
Model 1
0.0812
0.05 0.01*
1.48 0.71*
12.89 0.70*
1.53 0.50*
0.3225
0.05 0.01*
Adjusted also for physical activity, smoking status, and study site.
0.0520
lean mass with older age, but these were more similar in
Total fat2, kg
Comorbidity
Total fat, kg
(Tables 6 and 7). Age and higher body fat were inversely
associated with arm strength, although the effect of age
*P .05.
Black
R2
Table 4. Leg Muscle Quality (Nm/kg): Associations with Age, Race and Body Composition, Linear Regression Models
Men Women
Age 0.16 0.03* 0.17 0.03* 0.17 0.03* 0.15 0.03* 0.19 0.03* 0.12 0.03*
Black 0.59 0.18* 0.52 0.18* 0.84 0.16* 0.41 0.16* 0.33 0.16*
0.55 0.18*
Total fat, kg 0.12 0.05* 0.13 0.05* 0.09 0.04* 0.09 0.04*
Total fat2 0.004 0.001* 0.004 0.001* 0.003 0.001* 0.003 0.0006*
Comorbidity 0.16 0.08* 0.17 0.07*
R2 0.0273 0.0663 0.0731 0.0386 0.1187 0.1243
R2 Coefficient of determination.
* P .05.
in the models, although the moving average plots sug- strength. Comorbidity partly explained decreased arm
gested that those at the extremes of fat had lower arm strength and muscle quality with age. Together, these fac-
muscle quality. In women, the association between upper tors explained only a small part of the variance in muscle
extremity strength and race was diminished after adjust- strength, compared with the large effect of muscle mass.
ment for comorbidity. Similarly, arm muscle quality was Using different methods to measure muscle size or
inversely associated with age, fatness, race, and comorbid- lean mass, lower muscle mass in older adults has previ-
ity (Table 6 and 7). ously been well documented.1518 These data confirm that
All models were reexamined with different measures this lower muscle mass is a major factor for a lower
of adiposity substituted for percentage of body fat. Re- strength in old age. This suggests that efforts to preserve
gardless of the measure of adiposity (total weight, total fat lean mass itself should have a significant effect on preserv-
mass, BMI) there was an inverse quadratic association be- ing strength in old age. Given the restricted age range of
tween fatness and leg strength after adjustment for leg lean this cohort and that all participants were free of physical
mass and leg muscle quality. These associations were the limitation at baseline, relationships between age and
same when thigh muscle area ascertained by CT scan was strength or muscle quality were not expected. Age-related
substituted for lean mass (data not shown.) decrements in the quality of muscle have been described in
several other studies.48,19 Factors that account for this may
DISCUSSION include a decreased proportion of type II fibers, increased
This is the largest study to examine upper and lower ex- connective tissue, fatty infiltration, and altered muscle me-
tremity strength and muscle quality in well-functioning tabolism.20,21 Intervention studies have demonstrated that
community-dwelling older adults, including a large num- strength can be improved fairly dramatically, even if in-
ber of women and blacks. Previous work showing that creases in mass are small, suggesting that some aspect of
strength and muscle quality are lower at older ages were muscle quality can be modified.22,23 Modifiable risk factors
confirmed and extended. The data also suggest that high for the loss of muscle quality need to be identified and may
and low body fatness make an independent contribution differ from those that are associated with the loss of mus-
to the age-related decline in strength and muscle quality. cle mass.
However, lower leg lean mass and higher body fat did not The smaller effect of age on strength and muscle qual-
fully explain the association between age and lower leg ity in the upper extremities in men and women is largely
Table 5. Arm Strength, Muscle Mass, and Muscle Quality in Men and Women
Women Men
Grip strength, kg 23.26 5.32 26.02 6.95 24.48 6.25* 38.76 8.05 41.69 10.14 39.80 8.95*
Arm lean mass, kg 2.00 0.33 2.45 0.44 2.20 0.44* 3.51 0.53 3.91 0.66 3.66 0.61*
Specific force, kg force/kg mass 11.76 2.57 10.80 2.86 11.34 2.74* 11.10 2.15 10.76 2.54 10.98 2.30*
* Gender difference at P .001.
Racial difference at P .05.
328 NEWMAN ET AL. MARCH 2003VOL. 51, NO. 3 JAGS
0.20 0.05*
0.05 0.02*
0.48 0.15*
0.72 0.36*
5.87 0.46*
Model 4
0.2687
0.19 0.06*
0.06 0.02*
6.13 0.47*
0.27 0.37
Model 3
0.1815
Women
0.18 0.06*
5.44 0.42*
0.30 0.37
Model 2
0.1753
0.28 0.06*
2.70 0.34*
Table 6. Arm Strength (kg): Associations with Age, Race, and Body Composition (Linear Regression Models)
Model 1
0.0641
Standard Error
0.27 0.08*
0.20 0.04*
0.62 0.20*
0.19 0.51
7.05 0.43
Model 4
0.2963
0.32 0.08*
0.23 0.04*
7.52 0.43*
0.51 0.50
Model 3
0.2464
Men
0.33 0.08*
6.28 0.40*
0.31 0.49
Model 2
0.2188
0.0595
R2 Coefficient of determination.
* P 0.05.
Total fat
R2
Table 7. Muscle Quality (kg/kg): Associations with Age, Race, and Body Composition
Men Women
Age (year) 0.04 0.02 0.06 0.02* 0.04 0.02 0.05 0.03 0.08 0.03* 0.08 0.03*
Black race 0.36 0.14* 0.49 0.13* 0.48 0.13* 0.96 0.15* 0.65 0.15* 0.51 0.15*
Total fat 0.09 0.01* 0.09 0.01* 0.07 0.01* 0.07 0.01*
Comorbidity 0.17 0.06* 0.23 0.07*
Site 0.57 0.12* 1.13 0.14*
R2 0.0077 0.0842 0.1084 0.0323 0.0844 0.1366
* P .05.
Adjusted also for physical activity, smoking status, and study site.
R2 Coefficient of determination.
ference between this study and the BLSA is the truncated from the lean mass estimate, nor does it distinguish con-
age range presented here. In both studies, the different nective tissue from muscle tissue. This would not explain
methods of assessing strength in upper and lower extremi- these results, because those with both high and low fat had
ties may have influenced the results. lower muscle quality. In a related manuscript, the authors
Strength and muscle mass in older blacks has not been reported that a lower muscle density assessed by a lower
previously described. One study found that older blacks x-ray attenuation on CT scan attenuation accounts for
had a lower muscle mass adjusted for age, sex, and weight, part of the variation in strength and muscle quality, inde-
based on DEXA and total body potassium, but strength pendent of subcutaneous and intermuscular fat.13 More
was not measured in that study.25 Adjustment for body fat basic physiological work is needed to determine whether
and comorbidity, in addition to lean mass, attenuated but these findings reflect altered muscle metabolism, neuronal
did not eliminate the relationship between lower leg recruitment, or biomechanics.
strength and black race in the men in this study. It is pos- Several design features of this study must be consid-
sible that better measures of comorbidity or subclinical ered when interpreting these results. This cohort was se-
disease might explain this association with race. Although lected to examine risk factors for future disability, exclud-
more precise than anthropometry, DEXA may still not ing about 20% of older adults who have prevalent
fully capture important differences in body composition in impairment, reducing generalization to that group. Exclu-
men and women and those in different ethnic groups. It sions from strength testing for knee pain and other disease
has been proposed that DEXA more accurately captures further limit generalizability. However, the range of body
known ethnic differences in body composition than an- composition and the prevalence of other disease character-
thropometric measures,26 suggesting that the differences istics of this cohort have been well described and likely re-
observed here are less likely to be due to ethnic biases in flect the range of function of older adults being seen for
methodology than to other factors associated with race. It ambulatory medical care. Additionally, although both
is hoped that these more-specific measures of body com- blacks and whites selected were nondisabled, and adjust-
position might allow better identification of risk factors ments were made for potential confounders, there may
for loss of strength beyond the loss due to lower lean mass have been a differential rate in participation by race, and
per se.27 these biases cannot be excluded as an explanation for
The quadratic relationship between body fat and these findings. Finally, because strength was measured us-
strength is a unique finding that warrants further investi- ing a voluntary contraction, there may be motivational
gation. Those at the high and low extremes of percentage and biomechanical factors that are related to age, sex,
of body fat had lower levels of leg muscle quality than race, or degree of body fat that could explain these find-
those in the midrange. This effect was small, but of similar ings and that need to be explored further in studies of
magnitude to that of age itself in its effect on muscle qual- muscle physiology.
ity, in that the negative effect of a kg fat was similar to In summary, lower lean mass and strength were ob-
that of a year of age. Body fat has been shown to have an served across the eighth decade of age in the upper and
adverse effect on physical function.2,28 These data suggest lower extremities. Preservation of lean mass would be
that lower muscle quality in obese individuals may par- likely to have the greatest effect on the maintenance of
tially mediate this association. The optimal level of muscle strength in old age, but high or low body fat also has an
quality occurred at a much higher percentage of body fat adverse association with strength and muscle quality in
in women than in men. It may be that fat has positive and old age. Preservation of lean mass and prevention of gain
negative effects on preserving lean mass but decreasing in fat may both be important in preserving strength and
muscle quality.29 There may be a sex-specific range of muscle quality in old age. Future studies of the risk factors
body fat that is optimal for functioning. Lean mass mea- for loss of strength in old age must first carefully account
sured with DEXA does not exclude all intermuscular fat for the effects of body composition.
330 NEWMAN ET AL. MARCH 2003VOL. 51, NO. 3 JAGS
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